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The application of haplotypes instead of species-level ranks modifies the interpretation of ecological preferences in lichen symbiont interactions in Parmelia

. 2024 Aug 24 ; 14 (1) : 19682. [epub] 20240824

Language English Country England, Great Britain Media electronic

Document type Journal Article

Grant support
2012/07/N/NZ8/00061 Narodowe Centrum Nauki
BW/538-L150-B257-16 Wydział Biologii, Uniwersytet Gdański, Poland
RVO 67985939 Institute of Botany of the Czech Academy of Sciences

Links

PubMed 39181961
PubMed Central PMC11344855
DOI 10.1038/s41598-024-70667-1
PII: 10.1038/s41598-024-70667-1
Knihovny.cz E-resources

The analysis of the interaction between main bionts (mycobiont and photobiont) in the lichen symbiosis delivers substantial information about their preferences in the selection of symbiotic partners, and their ecological preferences. The selectivity in the Parmelia genus has been defined as strong so far. However, data on this lichen genus, which includes several widely distributed species, are biogeographically limited. Therefore, using specialization indicators and extended sampling, in this study, we estimated the interactions between the main bionts of selected Parmelia spp., using two levels of estimation (species/OTU and haplotype). A comparison of mycobiont-photobiont interactions at different levels showed that considering only mycobiont species and Trebouxia OTUs, greater specialization is found, while Parmelia species studied in this work present a more generalistic strategy in photobiont choice when haplotypes are considered. Despite the uneven sampling of Parmelia species, the interpretation of specialization within species and individuals of the genus leads to a more precise and accurate interpretation of their adaptation strategies. Furthermore, the data from P. sulcata indicate the existence of a different pool of compatible haplotypes in some geographical regions compared to neighboring areas. This observation suggests the potential influence of climatic factors.

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Tschermak-Woess, E. The algal partner. In CRC Handbook of Lichenology (ed. Gakum, M.) 39–92 (CRC Press, 1988).

Tschermak-Woess, E. Developmental studies in trebouxioid algae and taxonomical consequences. Plant Syst. Evol.164, 161–195 (1989).10.1007/BF00940436 DOI

Sanders, W. B. & Masumoto, H. Lichen algae: The photosynthetic partners in lichen symbioses. Lichenologist53, 347–393. 10.1017/S0024282921000335 (2021).10.1017/S0024282921000335 DOI

Hawksworth, D. L. & Grube, M. Lichens redefined as complex ecosystems. New Phytol.227, 1281–1283. 10.1111/nph.16630 (2020). 10.1111/nph.16630 PubMed DOI PMC

Mark, K. et al. Contrasting co-occurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species. New Phytol.227(5), 1–14. 10.1111/nph.16475 (2020).10.1111/nph.16475 PubMed DOI

Rodríguez-Arribas, C. et al. Specialization patterns in symbiotic associations: A community perspective over spatial scales. Ecol. Evol.13, e10296. 10.1002/ece3.10296 (2023). 10.1002/ece3.10296 PubMed DOI PMC

Beck, A., Kasalicky, T. & Rambold, G. Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytol.153, 317–326. 10.1046/j.0028-646X.2001.00315.x (2002).10.1046/j.0028-646X.2001.00315.x DOI

Kaasalainen, U., Tuovinen, V., Mwachala, G., Pellikka, P. & Rikkinen, J. Complex interaction networks among cyanolichens of a tropical biodiversity hotspot. Front. Microbiol.12, 1–12. 10.3389/fmicb.2021.672333 (2021).10.3389/fmicb.2021.672333 PubMed DOI PMC

Yahr, R., Vilgalys, R. & DePriest, P. T. Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol. Ecol.13, 3367–3378. 10.1111/j.1365-294X.2004.02350.x (2004). 10.1111/j.1365-294X.2004.02350.x PubMed DOI

Stenroos, S., Högnabba, F., Myllys, L., Hyvönen, J. & Thell, A. High selectivity in symbiotic associations of lichenized ascomycetes and cyanobacteria. Cladistics22, 230–238. 10.1111/j.1096-0031.2006.00101.x (2006).10.1111/j.1096-0031.2006.00101.x DOI

Leavitt, S. D. et al. Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota). Mol. Ecol.24, 3779–3797. 10.1111/mec.13271 (2015). 10.1111/mec.13271 PubMed DOI

Wornik, S. & Grube, M. Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microb. Ecol.59, 150–157. 10.1007/s00248-009-9584-y (2010). 10.1007/s00248-009-9584-y PubMed DOI

Otálora, M. A. G. et al. Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). Mol. Phylogenet. Evol.56(3), 1089–1095. 10.1016/j.ympev.2010.05.013 (2010). 10.1016/j.ympev.2010.05.013 PubMed DOI

Cao, S. et al. Distribution patterns of haplotypes for symbionts from Umbilicaria esculenta and U. muehlenbergii reflect the importance of reproductive strategy in shaping population genetic structure. BMC Microbiol.15, 1–212. 10.1186/s12866-015-0527-0 (2015). 10.1186/s12866-015-0527-0 PubMed DOI PMC

Steinová, J. et al. Reproductive and dispersal strategies shape the diversity of mycobiont–photobiont association in Cladonia lichens. Mol. Phylogenet. Evol.134, 226–237. 10.1016/j.ympev.2019.02.014 (2019). 10.1016/j.ympev.2019.02.014 PubMed DOI

Muggia, L., Grube, M. & Tretiach, M. Genetic diversity and photobiont associations in selected taxa of the Tephromela atra group (Lecanorales, lichenised Ascomycota). Mycol. Prog.7, 147–160. 10.1007/s11557-008-0560-6 (2008).10.1007/s11557-008-0560-6 DOI

Fedrowitz, K., Kaasalainen, U. & Rikkinen, J. Geographic mosaic of symbiont selectivity in a genus of epiphytic cyanolichens. Ecol Evol.9, 2291–2303. 10.1002/ece3.343 (2012).10.1002/ece3.343 PubMed DOI PMC

Singh, G. et al. Fungal–algal association patterns in lichen symbiosis linked to macroclimate. New Phytol.214, 317–329. 10.1111/nph.14366 (2017). 10.1111/nph.14366 PubMed DOI

Yahr, R., Vilgalys, R. & DePriest, P. T. Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol.172, 377–377. 10.1111/j.1469-8137.2006.01792.x (2006).10.1111/j.1469-8137.2006.01792.x PubMed DOI

Fernández-Mendoza, F. et al. Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol. Ecol.20, 1208–1232. 10.1111/j.1365-294X.2010.04993.x (2011). 10.1111/j.1365-294X.2010.04993.x PubMed DOI

Peksa, O. & Škaloud, P. Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol. Ecol.20(18), 3936–3948. 10.1111/j.1365-294X.2011.05168.x (2011). 10.1111/j.1365-294X.2011.05168.x PubMed DOI

Chagnon, P. L., Magain, N., Miadlikowska, J. & Lutzoni, F. Strong specificity and network modularity at a very fine phylogenetic scale in the lichen genus Peltigera. Oecologia187, 767–782. 10.1007/s00442-018-4159-6 (2018). 10.1007/s00442-018-4159-6 PubMed DOI

Pérez-Ortega, S. et al. Invariant properties of mycobiont-photobiont networks in Antarctic lichens. Glob. Ecol. Biogeogr.32, 2033–2046. 10.1111/geb.13744 (2023).10.1111/geb.13744 DOI

Hughes, J. B. The scale of resource specialization and the distribution and abundance of lycaenid butterflies. Oecologia123, 375–383. 10.1007/s004420051024 (2000). 10.1007/s004420051024 PubMed DOI

Schleuning, M. et al. Specialization of mutualistic interaction networks decreases toward tropical latitudes. Curr. Biol.22, 1925–1931. 10.1016/j.cub.2012.08.015 (2012). 10.1016/j.cub.2012.08.015 PubMed DOI

Maglianesi, M. A., Blüthgen, N., Böhning-Gaese, K. & Schleuning, M. Morphological traits determine specialization and resource use in plant–hummingbird networks in the neotropics. Ecology95, 3325–3334. 10.1890/13-2261.1 (2014).10.1890/13-2261.1 DOI

Ventre Lespiaucq, A., Jacquemyn, H., Rasmussen, H. N. & Méndez, M. Temporal turnover in mycorrhizal interactions: A proof of concept with orchids. New Phytol.230(5), 1690–1699. 10.1111/nph.17291 (2021). 10.1111/nph.17291 PubMed DOI

Devictor, V. et al. Defining and measuring ecological specialization. J. Appl. Ecol.47, 15–25. 10.1111/j.1365-2664.2009.01744.x (2010).10.1111/j.1365-2664.2009.01744.x DOI

Hale, M. E. A monograph of the lichen genus Parmelia Acharius sensu stricto (Ascomycotina: Parmeliaceae). Smithson. Contrib. Bot.66, 1–55. 10.5479/si.0081024X.66 (1987).10.5479/si.0081024X.66 DOI

Nash, T. H. Lichen Biology 2nd edn, 1–486 (Cambridge University Press, 2008).

Ossowska, E., Guzow-Krzemińska, B., Kolanowska, M., Szczepańska, K. & Kukwa, M. Morphology and secondary chemistry in species recognition of Parmelia omphalodes group—Evidence from molecular data with notes on the ecological niche modelling and genetic variability of photobionts. MycoKeys61, 39–74. 10.3897/mycokeys.61.38175 (2019). 10.3897/mycokeys.61.38175 PubMed DOI PMC

Moya, P. et al. Biodiversity patterns and ecological preferences of the photobionts associated with the lichen-forming genus Parmelia. Front. Microbiol.12, 765310. 10.3389/fmicb.2021.765310 (2021). 10.3389/fmicb.2021.765310 PubMed DOI PMC

Molina, M. C. et al. Neogene diversification in the temperate lichen-forming fungal genus Parmelia (Parmeliaceae, Ascomycota). Syst. Biodivers.15, 166–181. 10.1080/14772000.2016.1226977 (2017).10.1080/14772000.2016.1226977 DOI

Thell, A., Thor, G. & Ahti, T. In Parmelia in Nordic Lichen Flora, Volume 4: Parmeliaceae (eds Thell, A. & Moberg, R.) 83–90 (Nordic Lichen Society, 2011).

Feuerer, T. & Thell, A. Parmelia ernstiae—A new macrolichen from Germany. Mitt. Inst. Allg. Bot. Hamb.30–32, 49–60 (2002).

Molina, M. C., Crespo, A., Blanco, O., Lumbsch, H. T. & Hawksworth, D. L. Phylogenetic relationships and species concepts in Parmelia s.str. (Parmeliaceae) inferred from nuclear ITS rDNA and ß-tubulin sequences. Lichenologist36, 37–54. 10.1017/S0024282904013933 (2004).10.1017/S0024282904013933 DOI

Molina, M. C., Del-Prado, R., Divakar, P. K., Sanchez-Mata, D. & Crespo, A. Another example of cryptic diversity in lichen-forming fungi: The new species Parmelia mayi (Ascomycota: Parmeliaceae). Org. Divers. Evol.11, 331–342. 10.1007/s13127-011-0060-4 (2011).10.1007/s13127-011-0060-4 DOI

Crespo, A., Rico, V. J., Garrido, E., Lumbsch, H. T. & Divakar, P. K. A revision of species of the Parmelia saxatilis complex in the Iberian Peninsula with the description of P. rojoi, a new potentially relict species. Lichenologist52, 365–376. 10.1017/S0024282920000341 (2020).10.1017/S0024282920000341 DOI

Kurokawa, S. Japanese species of Parmelia Ach. (sens. Str.), Parmeliaceae (1). J. Jpn. Bot.69, 61–68 (1994).

Divakar, P. K., Molina, M. C., Lumbsch, H. T. & Crespo, A. Parmelia barrenoae, a new lichen species related to Parmelia sulcata (Parmeliaceae) based on molecular and morphological data. Lichenologist37, 37–46. 10.1017/S0024282904014641 (2005).10.1017/S0024282904014641 DOI

Molina, M. C. et al.Parmelia sulcata (Ascomycota: Parmeliaceae), a sympatric monophyletic species complex. Lichenologist43, 586–601. 10.1017/S0024282911000521 (2011).10.1017/S0024282911000521 DOI

Singh, G. et al. A glimpse into genetic diversity and symbiont interaction patterns in lichen communities from areas with different disturbance histories in Białowieża forest, Poland. Microorganisms7(335), 1–15. 10.3390/microorganisms7090335 (2019).10.3390/microorganisms7090335 PubMed DOI PMC

Romeike, J., Friedl, T., Helms, G. & Ott, S. Genetic diversity of algal and fungal partners in four species of Umbilicaria (Lichenized Ascomycetes) along a transect of the Antarctic Peninsula. Mol. Biol. Evol.19, 1209–1217. 10.1093/oxfordjournals.molbev.a004181 (2002). 10.1093/oxfordjournals.molbev.a004181 PubMed DOI

Lindgren, H. et al. High fungal selectivity for algal symbionts in the genus Bryoria. Lichenologist46, 681–695. 10.1017/S0024282914000279 (2014).10.1017/S0024282914000279 DOI

Hestmark, G., Lutzoni, F. & Miadlikowska, J. Photobiont associations in co-occurring umbilicate lichens with contrasting modes of reproduction in coastal Norway. Lichenologist48(5), 545–557. 10.1017/S0024282916000232 (2016).10.1017/S0024282916000232 DOI

Law, R. Evolution in a mutualistic environment. In The Biology of Mutualism: Ecology and Evolution (ed. Boucher, D.) 145–170 (Oxford University Press, 1985).

Ossowska, E., Guzow-Krzemińska, B., Dudek, M., Oset, M. & Kukwa, M. Evaluation of diagnostic chemical and morphological characters in five Parmelia species (Parmeliaceae, lichenized Ascomycota) with special emphasis on the thallus pruinosity. Phytotaxa383, 165–180. 10.11646/phytotaxa.383.2.3 (2018).10.11646/phytotaxa.383.2.3 DOI

Corsie, E. I., Harrold, P. & Yahr, R. No combination of morphological, ecological or chemical characters can reliably diagnose species in the Parmelia saxatilis aggregate in Scotland. Lichenologist51, 107–121. 10.1017/S0024282919000069 (2019).10.1017/S0024282919000069 DOI

Thell, A. et al. Notes on the systematics, chemistry and distribution of European Parmelia and Punctelia species (lichenized ascomycetes). Sauteria15, 545–559 (2008).

Muggia, L. et al. Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobiont genus Trebouxia (Trebouxiophyceae, Chlorophyta): An impetus for developing an integrated taxonomy. Mol. Phylogenet. Evol.149, 106821. 10.1016/j.ympev.2020.106821 (2020). 10.1016/j.ympev.2020.106821 PubMed DOI

Medeiros, I. D. et al. Turnover of Lecanoroid mycobionts and their Trebouxia photobionts along an elevation gradient in Bolivia highlights the role of environment in structuring the lichen symbiosis. Front. Microbiol.12, 774839. 10.3389/fmicb.2021.774839 (2021). 10.3389/fmicb.2021.774839 PubMed DOI PMC

Kosecka, M. et al. Phylogeny and ecology of Trebouxia photobionts from Bolivian lichens. Front. Microbiol.13, 779784. 10.3389/fmicb.2022.779784 (2022). 10.3389/fmicb.2022.779784 PubMed DOI PMC

Ossowska, E., Schiefelbein, U., Szymczyk, R. & Kukwa, M. Contribution to the knowledge of the distribution of Parmelia species (Parmeliaceae, Ascomycota)-new records confirmed by molecular data. Acta Mycol.58, 1–11. 10.5586/am/175356 (2023).10.5586/am/175356 DOI

Ossowska, E. A., Guzow-Krzemińska, B., Szymczyk, R. & Kukwa, M. A molecular re-evaluation of Parmelia encryptata with notes on its distribution. Lichenologist53, 341–345. 10.1017/S0024282921000219 (2021).10.1017/S0024282921000219 DOI

Castellani, M. B., Bianchi, E., Coppi, A., Nascimbene, J. & Benesperi, R. Revision of the Parmelia saxatilis group in Italy based on morphological, chemical, and molecular data. Phytotaxa512(1), 028–040. 10.11646/phytotaxa.512.1.2 (2021).10.11646/phytotaxa.512.1.2 DOI

Tsurykau, A., Bely, P., Golubkov, V., Persson, P.-E. & Thell, A. The lichen genus Parmelia (Parmeliaceae, Ascomycota) in Belarus. Herzogia32, 375–384. 10.13158/heia.32.2.2019.375 (2019).10.13158/heia.32.2.2019.375 DOI

Blüthgen, N., Menzel, F. & Blüthgen, N. Measuring specialization in species interaction networks. BMC Ecol.6, 9. 10.1186/1472-6785-6-9 (2006). 10.1186/1472-6785-6-9 PubMed DOI PMC

Piercey-Normore, M. D. & Depriest, P. T. Algal switching among lichen symbioses. Am. J. Bot.88(8), 1490–1498. 10.2307/3558457 (2001). 10.2307/3558457 PubMed DOI

Fründ, J., McCann, K. S. & Williams, N. M. Sampling bias is a challenge for quantifying specialization and network structure: Lessons from a quantitative niche model. Oikos125, 502–513. 10.1111/oik.02256 (2016).10.1111/oik.02256 DOI

Orange, A., James, P. W. & White, F. J. Microchemical Methods for the Identification of Lichens 1–101 (British Lichen Society, 2001).

White, T. J., Bruns, T., Lee, S. & Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In IPCR Protocols: A Guide to Methods and Applications (eds Innis, M. A. et al.) 315–322 (Academic Press, 1990).

Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts. Mol. Ecol.2, 113–118. 10.1111/j.1365-294x.1993.tb00005.x (1993). 10.1111/j.1365-294x.1993.tb00005.x PubMed DOI

Guzow-Krzemińska, B. Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist38(5), 469–476. 10.1017/S0024282906005068 (2006).10.1017/S0024282906005068 DOI

Helms, G., Friedl, T., Rambold, G. & Mayrhofer, H. Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing. Lichenologist33, 73–86. 10.1006/lich.2000.0298 (2001).10.1006/lich.2000.0298 DOI

Parker, S. R. AutoAssembler sequence assembly software. In Sequence Data Analysis Guidebook. Methods in Molecular Medicine™ (ed. Swindell, R.) 107–117 (Humana Press, 1997). PubMed

Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol.215, 403–410. 10.1016/S0022-2836(05)80360-2 (1990). 10.1016/S0022-2836(05)80360-2 PubMed DOI

Malíček, J., Palice, Z. & Vondrák, J. Additions and corrections to the lichen biota of the Czech Republic. Herzogia31, 453–475. 10.13158/heia.31.1.2018.453 (2018).10.13158/heia.31.1.2018.453 DOI

Crespo, A. et al. rDNA ITS and β-tubulin gene sequence analyses reveal two monophyletic groups within the cosmopolitan lichen Parmelia saxatilis. Mycol. Res.106(7), 788–795. 10.1017/S095375620200610X (2002).10.1017/S095375620200610X DOI

Muggia, L., Perez-Ortega, S., Fryday, A., Spribille, T. & Grube, M. Global assessment of genetic variation and phenotypic plasticity in the lichen forming species Tephromela atra. Fungal Divers.64, 233–251. 10.1093/aob/mcu146 (2014).10.1093/aob/mcu146 DOI

Ruprecht, U., Brunauer, G. & Printzen, C. Genetic diversity of photobionts in Antarctic lecideoid lichens from an ecological viewpoint. Lichenologist44, 661–678. 10.1017/S0024282912000291 (2012).10.1017/S0024282912000291 DOI

Nyati, S., Scherrer, S., Werth, S. & Honegger, R. Green-algal photobiont diversity (Trebouxia spp.) in representatives of Teloschistaceae (Lecanoromycetes, lichen-forming ascomycetes). Lichenologist46, 189–212. 10.1017/S0024282913000819 (2014).10.1017/S0024282913000819 DOI

Kroken, S. & Taylor, J. W. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist103, 645–660. 10.1639/0007-2745(2000)103[0645:PSRMAS]2.0.CO;2 (2000).10.1639/0007-2745(2000)103[0645:PSRMAS]2.0.CO;2 DOI

Dahlkild, Å. et al. Photobiont diversity in the Physciaceae (Lecanorales). Bryologist104, 527–553. 10.1639/0007-2745(2001)104[0527:PDITPL]2.0.CO;2 (2001).10.1639/0007-2745(2001)104[0527:PDITPL]2.0.CO;2 DOI

Friedl, T., Besendahl, A., Pfeiffer, P. & Bhattacharya, D. The distribution of group I introns in lichen algae suggests that lichenization facilitates intron lateral transfer. Mol. Phylogenet. Evol.14(3), 342–352. 10.1006/mpev.1999.0711 (2000). 10.1006/mpev.1999.0711 PubMed DOI

Werth, S. Fungal-algal interactions in Ramalina menziesii and its associated epiphytic lichen community. Lichenologist44(4), 543–560. 10.1017/S0024282912000138 (2012).10.1017/S0024282912000138 DOI

Altermann, S., Leavitt, S. D. & Goward, T. Tidying up the genus Letharia: Introducing L. lupina sp. Nov. and a new circumscription for L. columbiana. Lichenologist48(5), 423–439. 10.1017/S0024282916000396 (2016).10.1017/S0024282916000396 DOI

Sadowska-Deś, A. D., Bálint, M., Otte, J. & Schmitt, I. Assessing intraspecific diversity in a lichen-forming fungus and its green algal symbiont: Evaluation of eight molecular markers. Fungal Ecol.6, 141–151. 10.1016/J.FUNECO.2012.12.001 (2013).10.1016/J.FUNECO.2012.12.001 DOI

Domaschke, S., Fernández-Mendoza, F., García, M. A., Martín, M. P. & Printzen, C. Low genetic diversity in Antarctic populations of the lichen-forming ascomycete Cetraria aculeata and its photobiont. Polar Res.31(1), 17353. 10.3402/polar.v31i0.17353 (2012).10.3402/polar.v31i0.17353 DOI

del Campo, E. M., del Hoyo, A., Casano, L. M., Martínez-Alberola, F. & Barreno, E. A rapid and cost-efficient DMSO-based method for isolating DNA from cultured lichen photobionts. Taxon59, 588–591. 10.1002/tax.592023 (2010).10.1002/tax.592023 DOI

Pérez-Ortega, S., Ortiz-Álvarez, R., Allan Green, T. G. & de Los Ríos, A. Lichen myco- and photobiont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiol. Ecol.82(2), 429–448. 10.1111/j.1574-6941.2012.01422.x (2012). 10.1111/j.1574-6941.2012.01422.x PubMed DOI

Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res.30, 3059–3066. 10.1093/nar/gkf436 (2002). 10.1093/nar/gkf436 PubMed DOI PMC

Landan, G. & Graur, D. Local reliability measures from sets of co-optimal multiple sequence alignments. Pac. Symp. Biocomput.13, 15–24 (2008). PubMed

Penn, O. et al. GUIDANCE: A web server for assessing alignment confidence scores. Nucleic Acids Res.38, W23–W28. 10.1093/nar/gkq443 (2010). 10.1093/nar/gkq443 PubMed DOI PMC

Sela, I., Ashkenazy, H., Katoh, K. & Pupko, T. GUIDANCE2: Accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res.43, W7–W14. 10.1093/nar/gkq443 (2015). 10.1093/nar/gkq443 PubMed DOI PMC

Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol. Biol. Evol.32, 268–274. 10.1093/molbev/msu300 (2015). 10.1093/molbev/msu300 PubMed DOI PMC

Chernomor, O., von Haeseler, A. & Minh, B. Q. Terrace aware data structure for phylogenomic inference from supermatrices. Syst. Biol.65, 997–1008. 10.1093/sysbio/syw037 (2016). 10.1093/sysbio/syw037 PubMed DOI PMC

Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods14(6), 587–589. 10.1038/nmeth.4285 (2017). 10.1038/nmeth.4285 PubMed DOI PMC

Hoang, D. T., Chernomor, O., Von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: Improving the ultrafast bootstrap approximation. Mol. Biol. Evol.35(2), 518–522. 10.1093/molbev/msx281 (2018). 10.1093/molbev/msx281 PubMed DOI PMC

Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. Partition Finder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol.34(3), 772–773. 10.1093/molbev/msw260 (2016).10.1093/molbev/msw260 PubMed DOI

Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES science gateway for inference of large phylogenetic trees. In 2010 Gateway Computing Environments Workshop (GCE) 1–8 (IEEE, 2010).

Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics17, 754–755. 10.1093/bioinformatics/17.8.754 (2001). 10.1093/bioinformatics/17.8.754 PubMed DOI

Ronquist, H. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics19, 1572–1574 (2003). 10.1093/bioinformatics/btg180 PubMed DOI

Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci.7(4), 457–472. 10.1214/ss/1177011136 (1992).10.1214/ss/1177011136 DOI

Rambaut A. FigTreev1.4.4. http://tree.bio.ed.ac.uk/software/figtree/. Accessed on 12 Apr 2021. (2021).

Aktas, C. Haplotypes: Haplotype Inference and Statistical Analysis of Genetic Variation. R Package Version 1.0. Available online: https://CRAN.R-project.org/package=haplotypes, accessed on 1 November 2018 (2015).

Clement M, Snell Q, Walker P, Posada D, Crandall K. TCS: Estimating gene genealogies. Parallel and Distributed Processing Symposium, International Proceedings, 2, 184. (2002).

Dormann, C. F., Gruber, B. & Fründ, J. Introducing the bipartite package: Analysing ecological networks. R News8, 2413793 (2008).

Dunne, J. A., Williams, R. J. & Martinez, N. D. Food-web structure and network theory: The role of connectance and size. Proc. Natl. Acad. Sci. U. S. A.99(20), 12917–12922. 10.1073/pnas.192407699 (2002). 10.1073/pnas.192407699 PubMed DOI PMC

Krebs, C. J. Ecological Methodology (Harper Collins, 1989).

R Core Team. R: A Language and Environment for Statistical Computing. Available online: https://www.Rproject.org/, accessed on 1 January 2019 (2017).

RStudio Team. RStudio: Integrated Development for R. RStudio, Inc., Boston, MA. Available online: http://www.rstudio.com/, accessed on 1 January 2019 (2018).

Vu VQ, Friendly M. ggbiplot: A Grammar of Graphics Implementation of Biplots. Available online: https://github.com/friendly/ggbiplot, accessed on 1 July 2024 (2023).

Fick, S. E. & Hijmans, R. J. WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol.37, 4302–4315. 10.1002/joc.5086 (2017).10.1002/joc.5086 DOI

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